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Force transmission during adhesion-independent migration

Nature Cell Biology volume 17, pages 524–529 (2015)Cite this article

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Abstract

When cells move using integrin-based focal adhesions, they pull in the direction of motion with large, ∼100 Pa, stresses that contract the substrate1. Integrin-mediated adhesions, however, are not required for in vivo confined migration2. During focal adhesion-free migration, the transmission of propelling forces, and their magnitude and orientation, are not understood. Here, we combine theory and experiments to investigate the forces involved in adhesion-free migration. Using a non-adherent blebbing cell line as a model, we show that actin cortex flows drive cell movement through nonspecific substrate friction. Strikingly, the forces propelling the cell forward are several orders of magnitude lower than during focal-adhesion-based motility. Moreover, the force distribution in adhesion-free migration is inverted: it acts to expand, rather than contract, the substrate in the direction of motion. This fundamentally different mode of force transmission may have implications for cell–cell and cell–substrate interactions during migration in vivo.

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Figure 1: Specific-adhesion-independent migration of blebbing Walker cells in confined environments.
Figure 2: A minimum friction is required for cortical flow-driven migration of non-adherent Walker cells.
Figure 3: The mechanics of specific-adhesion-independent migration.
Figure 4: Force distribution underlying migration in the absence of specific adhesion.

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Acknowledgements

We thank K. J. Chalut, M. Raff, L. Rohde and the members of the Paluch laboratory for comments on the manuscript. This work was supported by the Polish Ministry of Science and Higher Education (grant 454/N-MPG/2009/0 to E.K.P.), thanks to the International Institute of Molecular and Cell Biology in Warsaw, the European Research Council (ERC starting grant 311637-MorphCorDiv to E.K.P.), the Medical Research Council UK (core funding to the LMCB, M.B., I.M.A. and E.K.P. and award MC_UP_1202/3 to A.C.O.), the Max Planck Society (A.C.O., E.K.P. and G.S.), the German Research Foundation (DFG-GSC 97/3 to A.E.), the Whitaker International Program (R.A.D.), the Wellcome Trust (WT098025MA, R.A.D. and A.C.O.) and the Royal Society (University Research Fellowship to G.C.).

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Author notes

  1. Martin Bergert

    Present address: Present address: Laboratory of Thermodynamics in Emerging Technologies, ETH Zürich 8092 Zürich, Switzerland.,

  2. Martin Bergert and Anna Erzberger: These authors contributed equally to this work.

Authors and Affiliations

  1. MRC Laboratory for Molecular Cell Biology, UCL, London WC1E 6BT, UK

    Martin Bergert, Irene M. Aspalter & Ewa K. Paluch

  2. Institute for the Physics of Living Systems, UCL, London WC1E 6BT, UK

    Martin Bergert, Ravi A. Desai, Irene M. Aspalter, Andrew C. Oates, Guillaume Charras & Ewa K. Paluch

  3. Max Planck Institute for the Physics of Complex Systems, Dresden 01187, Germany

    Anna Erzberger & Guillaume Salbreux

  4. MRC National Institute for Medical Research, London NW7 1AA, UK

    Ravi A. Desai & Andrew C. Oates

  5. Department of Cell and Developmental Biology, UCL, London WC1E 6BT, UK

    Ravi A. Desai & Andrew C. Oates

  6. London Centre for Nanotechnology and Department of Cell and Developmental Biology, UCL, London WC1H 0AH, UK

    Guillaume Charras

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Contributions

M.B., A.E., G.S. and E.K.P. designed the research and wrote the paper, M.B. performed the experiments, M.B. and A.E. analysed the data and A.E. and G.S. developed the theoretical model. M.B. and R.A.D. designed the microfluidic assays and performed microfabrication. I.M.A. helped to perform revision experiments. G.C. and A.C.O. gave technical support and conceptual advice. All authors discussed the results and implications and commented on the manuscript at all stages.

Corresponding authors

Correspondence to Guillaume Salbreux or Ewa K. Paluch.

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Integrated supplementary information

Supplementary Figure 1 Blebbing Walker cell migration is focal adhesion independent but depends on a rearward myosin contractility gradient.

a, Snapshot and kymograph of a blebbing Walker cell in microchannel (8 × 8 μm) coated with 50 μg ml−1β-Lactoglobulin. Scale bars: horizontal: 10 μm, vertical: 50 s. b, Plot shows instantaneous velocity of Walker cells in microchannels coated with 50 μg ml−1 BSA or β-Lactoglobulin. P-value: Welch’s two-sided t-test, n: number of cells analysed in 2 (BSA) and 3 (β-Lactoglobulin) independent experiments. Boxes in boxplots extend from the 25th to 75th percentiles, with a line at the median. Whiskers extend to 1.5× IQR (interquartile range) or the max/min datapoints. c, Blebbing Walker cells expressing GFP-FAK do not form detectable focal adhesions during migration under agarose, while adherent Walker cells show focal adhesions during 2D migration on glass. Arrows indicate migration direction. Scale bars: 10 μm. d, Tracks of migrating blebbing Walker cells under agarose on glass, PEG-coated glass and commercially available low attachment surfaces. Cells were manually tracked for 52 min. Scale bars: 50 μm. e, Under agarose migration velocity of cells with reduced Talin expression levels (see also Supplementary Fig. 5). P-value: Welch’s two-sided t-test, n: number of cells analysed in 2 independent experiments. Boxes in boxplots extend from the 25th to 75th percentiles, with a line at the median. Whiskers extend to 1.5× IQR (interquartile range) or the max/min datapoints. f, Double laser ablation of the actomyosin cortex at the rear of the cell body (highest Myosin and F-Actin intensities) caused an instantaneous, strong decrease in cell velocity compared to a double ablation at the cell front. Scale bars: horizontal: 10 μm, vertical: 50 s. Plot shows reduction in cell velocity in % relative to the pre-ablation velocity. Horizontal bars: mean values. P-value: Welch’s two-sided t-test; n: number of cells analysed in 3 (rear) and 2 (front) independent experiments. g, Confocal images of Walker cells labelled with MRLC-GFP: upper panel: cortex section, lower panel: middle cross section. Scale bar: 10 μm. The white rectangles highlight the ROI chosen for the analysis of myosin II intensity. h, To obtain cortical myosin intensity profiles (panel i), we subtracted the normalized fluorescence intensity profile in the middle cell section (cytoplasmic background, grey) from the myosin intensity profile acquired at the cell surface (black). n = 33 cells from 5 independent experiments. (i), Relative myosin fluorescence intensity profiles at the cortex for different friction conditions. n: number of cells analysed in 5 (BSA), 3 (BSA/F127) and 5 (F127) independent experiments All error bars: SEM

Supplementary Figure 2 Varying and measuring substrate friction.

a, Design of the microfluidic chip used for friction measurements. 3 entry ports were connected to reservoirs. Blowup shows region with bypass (h: 8 μm, w: 50 μm) and analysis channel (h: 8 μm, w: 8 μm). Micrograph shows single cell entering the analysis channel. Scale bar: 10 μm. b, Schematic of the measurement setup and principle of flow control. The pressure difference and thus the flow were controlled by adjusting the height of reservoir E3 relative to the other reservoirs E1 and E2. c, Calibration of the free average flow in the microfluidic friction device based on tracking of fluorescent beads. n: number of measurements pooled from several independent experiments as indicated in the figure. d, Maximum intensity projections of Z-stacks taken at the entry regions to microchannels coated with 50 μg ml−1 fluorescent BSA-488 mixed with 0 μg ml−1, 30 μg ml−1 or 200 μg ml−1 F127. Scale bars: 10 μm e–g, Cell velocities and linear fits in microfluidic friction devices coated with F127, BSA-F127 mix or BSA. Error bars represent SEMs. For e n = 9 cells analysed from 3 independent experiments; for f n = 10 cells analysed from 2 independent experiments; for g n = 9 cells analysed from 3 independent experiments. h. Cell substrate friction coefficient measured for channels coated with F127, BSA-F127-mix and BSA. n: number of cells analysed from 3 (F127), 2 (BSA/F127) and 3 (BSA) independent experiments.

Supplementary Figure 3 Mechanical description of focal adhesion-independent migration.

a, Contact between a Walker cell and the channel wall visualized using interference reflection microscopy (IRM). Scale bar: 10 μm. b, Upper panel: Time-average (3 min) maximum intensity projection of the surface of a cell expressing MRLC-GFP. On timescales exceeding the bleb life cycle, the cell front has a near-hemispherical average shape. Scale bar: 10 μm. Lower panel: Parametrization and geometry of the axisymmetric cell surface. c, Coordinates used in different cell parts. d, Upper panel: Linear profile of myosin-generated active tension ζ(x) along the cell axis used for analytical calculations. Lower panel: Retrograde cortical flow profiles along the cell (reference frame of the cell). The cortical flow velocity depends on the friction coefficient. [vnorm = (ζ(r) − ζ(f))L/η]. e, Cell velocity and external pressure. Upper panel: Schematic of internal and external pressures acting on the cell. Lower panel: Relation between cell velocity and external pressure difference shown for the parameter values in Table 1 (Supplementary Note). The stalling pressure of −15 Pa is three orders of magnitude lower than reported values for adhesive cells in micropipettes (around −2 kPa Supplementary Note Reference 17). f, Upper panel: Schematic of the frictional and drag forces acting on the cell in the absence of an external pressure difference. In the region where the cell contacts the channel wall, relative flow of the cortex to the wall generates frictional force. At the pole regions, fluid drag forces exerted by the surrounding medium oppose propulsive frictional forces. Lower panel: Cell velocity (solid lines) and maximum cortex velocity relative to the channel wall (dashed lines) as a function of the friction coefficient α and the drag coefficient αD. Cell motion occurs above a threshold friction α∗, set by the fluid drag coefficient: when friction is too small, cells cannot migrate against the drag force exerted by the fluid in the channel. g, Comparison between numerical evaluation of the inflexion point of the cell velocity U(α) (dots) and the proposed approximate relation α∗ = RαD/(2L) (line), see Eq. 49. [αnorm = η/L2]. Red dot: value obtained from the fitting procedure to experimental data.

Supplementary Figure 4 Role of the nucleus and internal friction (a–d), hydraulics of the channel-cell system (e), validation of the estimated fluid drag coefficient (f–h) and forces exerted on the channel walls (i).

(a), Quantification of nuclear cross-sectional area. Scale bar: 10 μm. b, c, Nuclear cross-sectional area does not correlate with cell velocity in intermediate (b) or high (c) friction channels. NExp = 1(b) or 4(c). (d), Schematic of internal friction arising from intracellular material. In this description, the intracellular pressure difference between the rear and front of the migrating cell is balanced by the frictional forces fint exerted by the actin cortex (see SI section 4.2). (e), A single cell migrating in a channel experiences drag forces governed by the fluid flow resistances in the channel. A channel segment containing a cell offers a flow resistance ξ while the fluid-filled channel is characterized by the resistance ξc. When multiple cells migrate in a channel, the fluid drag coefficient depends predominantly on the flow resistance of cell segments ξ. For definition of the fluid flow resistances of the rear and front part of the channel ξc(r) and ξc(f) see Equations 51-52. (f), Average fluid flow velocity induced by migrating cells was estimated by tracking microspheres in channels with rapidly migrating cells. Scale bar: 10 μm. (g), Kymograph of BSA-coated microchannel array with multiple migrating cells labelled with MRLC-GFP. Scale bars: horizontal: 500 μm, vertical: 30 min. (h), Histogram of cell velocities in BSA-coated channels obtained from kymographs of the full microchannel array. To allow for comparison with fluid flow measurements in channels with rapidly migrating cells, time-windows without cell velocities above 5.45 μm min−1 were discarded. The threshold was chosen according to the 0.1 quantile of the velocity distribution of polarised, fast cells used for cortical flow analysis. n = 164 cells from 2 independent experiments. (i), Distribution of forces exerted by migrating Walker cells on the channel wall in large, intermediate and small friction channels. Cell migration direction is to the right, the force is oriented on average in the direction opposite to cell motion, and the stress magnitudes are in the mPa-Pa range.

Supplementary Figure 5 Uncropped Western Blots and images of molecular weight makers.

Dashed lines indicate how the blot was cropped in Supplementary Fig. 1e.

Supplementary information

Supplementary Information

Supplementary Information (PDF 1364 kb)

Migration of blebbing Walker cell in collagen gel in the presence of EDTA.

Blebbing Walker cell migrating in a three-dimensional collagen gel in the presence of 2 mM EDTA. Scale bar: 10 μm; 25 s/frame; DIC, confocal microscopy (Lifeact-mCherry, maximum intensity projection) and confocal reflection microscopy (collagen fibres). (MOV 3216 kb)

Migration of a non-adherent Walker cell in a BSA-coated microchannel.

Non-adherent Walker cell placed in a microchannel (10 μm × 8 μm) coated with BSA in the presence of 50 μm CK-666. Scale bar: 10 μm; 5 s/frame; phase contrast. (MOV 496 kb)

Ablation of the cortex in the rear part of a non-adherent Walker cell in a microchannel.

Non-adherent Walker cell expressing Lifeact-mCherry in a BSA-coated microchannel (6 μm × 8 μm) in the presence of 50 μm CK-666. The cortex at the rear of the cell body was ablated twice. Scale bar: 10 μm; 1 s/frame; DIC and confocal microscopy (Lifeact-mCherry). (MOV 1037 kb)

Ablation of the cortex at the leading edge of a non-adherent Walker cell in a microchannel.

Blebbing Walker cell expressing Lifeact-mCherry in a BSA-coated microchannel (6 μm × 8 μm) in the presence of 50 μm CK-666. The cortex at the leading edge was ablated twice. Scale bar: 10 μm; 1 s/frame; DIC and confocal microscopy (Lifeact-mCherry). (MOV 1383 kb)

F-Actin dynamics at the cortex of a Walker cell migrating in a BSA-coated channel.

F-Actin dynamics in a non-adherent Walker cell expressing Lifeact-GFP in a BSA-coated microchannel (8 μm × 6 μm) in the presence of 50 μm CK-666. Scale bar: 10 μm; 2 s/frame; DIC and confocal microscopy (Lifeact-GFP). Left: images in the reference frame of the channel; right: images in the reference frame of the cell. (MOV 2477 kb)

Myosin dynamics at the cortex of a Walker cell migrating in a BSA-coated channel.

Myosin dynamics in a non-adherent Walker cell expressing MRLC-GFP in a BSA-coated microchannel (10 μm × 6 μm) in the presence of 50 μm CK-666. Scale bar: 10 μm; 2 s/frame; DIC and confocal microscopy (MRLC-GFP). Left: images in the reference frame of the channel; right: images in the reference frame of the cell. (MOV 2751 kb)

Microfluidic-based friction measurements.

Summary of performed friction measurements. The microfluidic device in this example was coated with F127. Scale bar: 10 μm; confocal microscopy (beads) or phase contrast (cells). (MOV 12311 kb)

Non-adherent Walker cell in an F127-coated microchannel (low friction).

Non-adherent Walker cell placed in a microchannel (10 μm × 8 μm) coated with F127 in the presence of 50 μm CK-666. The cell is polarized but does not migrate. Scale bar: 10 μm; 5 s/frame; phase contrast. (MOV 275 kb)

Myosin dynamics at the cortex of a Walker cell in an F127-coated channel (low friction).

Myosin dynamics in a non-adherent Walker cell expressing MRLC-GFP in a F127-coated microchannel (10 μm × 6 μm) in the presence of 50 μm CK-666. Scale bar: 10 μm; 2 s/frame; DIC and confocal microscopy (MRLC-GFP). Images in the reference frame of the channel. (MOV 1036 kb)

Myosin dynamics at the cortex of a Walker cell migrating in a channel with intermediate friction.

Myosin dynamics in a non-adherent Walker cell expressing MRLC-GFP in a microchannel coated with a mix of BSA and F127 (10 μm × 6 μm) in the presence of 50 μm CK-666. Scale bar: 10 μm; 2 s/frame; DIC and confocal microscopy (MRLC-GFP). Images in the reference frame of the channel. (MOV 1216 kb)

Simulation of cell motion and cortical flow velocity predicted by the theoretical description of flow-friction based cell migration.

Simulations are shown for the three different values of friction measured in F127, F127/BSA and BSA coated channels respectively (from top to bottom). Black dots at the cell surface depict cortex flows. (MOV 3444 kb)

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Bergert, M., Erzberger, A., Desai, R. et al. Force transmission during adhesion-independent migration. Nat Cell Biol 17, 524–529 (2015). https://doi.org/10.1038/ncb3134

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